Pulsatile modulation greatly enhances neural synchronization at syllable rate in children.

Neural processing of the speech envelope is of crucial importance for speech perception and comprehension. This envelope processing is often investigated by measuring neural synchronization to sinusoidal amplitude-modulated stimuli at different modulation frequencies. However, it has been argued that these stimuli lack ecological validity. Pulsatile amplitude-modulated stimuli, on the other hand, are suggested to be more ecologically valid and efficient, and have increased potential to uncover the neural mechanisms behind some developmental disorders such a dyslexia. Nonetheless, pulsatile stimuli have not yet been investigated in pre-reading and beginning reading children, which is a crucial age for developmental reading research. We performed a longitudinal study to examine the potential of pulsatile stimuli in this age range. Fifty-two typically reading children were tested at three time points from the middle of their last year of kindergarten (5 years old) to the end of first grade (7 years old). Using electroencephalography, we measured neural synchronization to syllable rate and phoneme rate sinusoidal and pulsatile amplitude-modulated stimuli. Our results revealed that the pulsatile stimuli significantly enhance neural synchronization at syllable rate, compared to the sinusoidal stimuli. Additionally, the pulsatile stimuli at syllable rate elicited a different hemispheric specialization, more closely resembling natural speech envelope tracking. We postulate that using the pulsatile stimuli greatly increases EEG data acquisition efficiency compared to the common sinusoidal amplitude-modulated stimuli in research in younger children and in developmental reading research.

Atypical neural processing of rise time by adults with dyslexia.

In recent studies phonological deficits in dyslexia are related to a deficit in the synchronization of neural oscillations to the dynamics of the speech envelope. The temporal features of both amplitude modulations and rise times characterize the speech envelope. Previous studies uncovered the inefficiency of the dyslexic brain to follow different amplitude modulations in speech. However, it remains to be investigated how the envelope's rise time mediates this neural processing. In this study we examined neural synchronization in students with and without dyslexia using auditory steady-state responses at theta, alpha, beta and low-gamma range oscillations (i.e., 4, 10, 20 and 40 Hz) to stimuli with different envelope rise times. Our results revealed reduced neural synchronization in the alpha, beta and low-gamma frequency ranges in dyslexia. Moreover, atypical neural synchronization was modulated by rise time for alpha and beta oscillations, showing that deficits found at 10 and 20 Hz were only evident when the envelope's rise time was significantly shortened. This impaired tracking of rise time cues may very well lead to the speech and phonological processing difficulties observed in dyslexia.

Theta, beta and gamma rate modulations in the developing auditory system.

In the brain, the temporal analysis of many important auditory features relies on the synchronized firing of neurons to the auditory input rhythm. These so-called neural oscillations play a crucial role in sensory and cognitive processing and deviances in oscillatory activity have shown to be associated with neurodevelopmental disorders. Given the importance of neural auditory oscillations in normal and impaired sensory and cognitive functioning, there has been growing interest in their developmental trajectory from early childhood on. In the present study, neural auditory processing was investigated in typically developing young children (n = 40) and adults (n = 27). In all participants, auditory evoked theta, beta and gamma responses were recorded. The results of this study show maturational differences between children and adults in neural auditory processing at cortical as well as at brainstem level. Neural background noise at cortical level was shown to be higher in children compared to adults. In addition, higher theta response amplitudes were measured in children compared to adults. For beta and gamma rate modulations, different processing asymmetry patterns were observed between both age groups. The mean response phase was also shown to differ significantly between children and adults for all rates. Results suggest that cortical auditory processing of beta develops from a general processing pattern into a more specialized asymmetric processing preference over age. Moreover, the results indicate an enhancement of bilateral representation of monaural sound input at brainstem with age. A dissimilar efficiency of auditory signal transmission from brainstem to cortex along the auditory pathway between children and adults is suggested. These developmental differences might be due to both functional experience-dependent as well as anatomical changes. The findings of the present study offer important information about maturational differences between children and adults for responses to theta, beta and gamma rates. The current study can have important implications for the understanding of developmental disorders which are known to be associated with deviances in neural auditory processing.

White matter lateralization and interhemispheric coherence to auditory modulations in normal reading and dyslexic adults.

Neural activation of slow acoustic variations that are important for syllable identification is more lateralized to the right hemisphere than activation of fast acoustic changes that are important for phoneme identification. It has been suggested that this complementary function at different hemispheres is rooted in a different degree of white matter myelination in the left versus right hemisphere. The present study will investigate this structure-function relationship with Diffusion Tensor Imaging (DTI) and Auditory Steady-State Responses (ASSR), respectively. With DTI we examined white matter lateralization in the cortical auditory and language regions (i.e. posterior region of the superior temporal gyrus and the arcuate fasciculus) and white matter integrity in the splenium of the corpus callosum. With ASSR we examined interhemispheric coherence to slow, syllabic-rate (i.e. 4 Hz) and fast, phonemic-rate (i.e. 20 Hz) modulations. These structural and functional techniques were applied in a group of normal reading adults and a group of dyslexic adults for whom previously reduced functional interhemispheric connectivity at 20 Hz has been reported (Poelmans et al. (2012). Ear and Hearing, 33, 134-143). This sample was chosen since it is hypothesized that in dyslexic readers insufficient hemispheric asymmetry in myelination might relate to their auditory and phonological problems. Results demonstrate reduced white matter lateralization in the posterior superior temporal gyrus and the arcuate fasciculus in the dyslexic readers. Additionally, white matter lateralization in the posterior superior temporal gyrus and white matter integrity in the splenium of the corpus callosum related to interhemispheric coherence to phonemic-rate modulations (i.e. 20 Hz). Interestingly, this correlation pattern was opposite in normal versus dyslexic readers. These results might imply that less pronounced left white matter dominance in dyslexic adults might relate to their problems to process phonemic-rate acoustic information and to integrate them into the phonological system.

Hemispheric asymmetry of auditory steady-state responses to monaural and diotic stimulation.

Amplitude modulations in the speech envelope are crucial elements for speech perception. These modulations comprise the processing rate at which syllabic (~3-7 Hz), and phonemic transitions occur in speech. Theories about speech perception hypothesize that each hemisphere in the auditory cortex is specialized in analyzing modulations at different timescales, and that phonemic-rate modulations of the speech envelope lateralize to the left hemisphere, whereas right lateralization occurs for slow, syllabic-rate modulations. In the present study, neural processing of phonemic- and syllabic-rate modulations was investigated with auditory steady-state responses (ASSRs). ASSRs to speech-weighted noise stimuli, amplitude modulated at 4, 20, and 80 Hz, were recorded in 30 normal-hearing adults. The 80 Hz ASSR is primarily generated by the brainstem, whereas 20 and 4 Hz ASSRs are mainly cortically evoked and relate to speech perception. Stimuli were presented diotically (same signal to both ears) and monaurally (one signal to the left or right ear). For 80 Hz, diotic ASSRs were larger than monaural responses. This binaural advantage decreased with decreasing modulation frequency. For 20 Hz, diotic ASSRs were equal to monaural responses, while for 4 Hz, diotic responses were smaller than monaural responses. Comparison of left and right ear stimulation demonstrated that, with decreasing modulation rate, a gradual change from ipsilateral to right lateralization occurred. Together, these results (1) suggest that ASSR enhancement to binaural stimulation decreases in the ascending auditory system and (2) indicate that right lateralization is more prominent for low-frequency ASSRs. These findings may have important consequences for electrode placement in clinical settings, as well as for the understanding of low-frequency ASSR generation.

A tractography study in dyslexia: neuroanatomic correlates of orthographic, phonological and speech processing.

Diffusion tensor imaging tractography is a structural magnetic resonance imaging technique allowing reconstruction and assessment of the integrity of three dimensional white matter tracts, as indexed by their fractional anisotropy. It is assumed that the left arcuate fasciculus plays a crucial role for reading development, as it connects two regions of the reading network, the left temporoparietal region and the left inferior frontal gyrus, for which atypical functional activation and lower fractional anisotropy values have been reported in dyslexic readers. In addition, we explored the potential role of the left inferior fronto-occipital fasciculus, which might connect a third region of the reading network, the left ventral occipitotemporal region with the left inferior frontal gyrus. In the present study, 20 adults with dyslexia and 20 typical reading adults were scanned using diffusion tensor imaging, and the bilateral arcuate fasciculus and the left inferior fronto-occipital fasciculus were delineated. Group comparisons show a significantly reduced fractional anisotropy in the left arcuate fasciculus of adults with dyslexia, in particular in the segment that directly connects posterior temporal and frontal areas. This fractional anisotropy reduction might reflect a lower degree of myelination in the dyslexic sample, as it co-occurred with a group difference in radial diffusivity. In contrast, no significant group differences in fractional anisotropy were found in the right arcuate fasciculus or in the left inferior fronto-occipital fasciculus. Correlational analyses (controlled for reading status) demonstrated a specific relation between performance on phoneme awareness and speech perception and the integrity of left arcuate fasciculus as indexed by fractional anisotropy, and between orthographic processing and fractional anisotropy values in left inferior fronto-occipital fasciculus. The present study reveals structural anomalies in the left arcuate fasciculus in adults with dyslexia. This finding corroborates current hypotheses of dyslexia as a disorder of network connections. In addition, our study demonstrates a correlational double dissociation, which might reflect neuroanatomical correlates of the dual route reading model: the left arcuate fasciculus seems to sustain the dorsal phonological route underlying grapheme-phoneme decoding, while the left inferior fronto-occipital fasciculus seems to sustain the ventral orthographic route underlying reading by direct word access.

Impairments in speech and nonspeech sound categorization in children with dyslexia are driven by temporal processing difficulties.

Auditory processing problems in persons with dyslexia are still subject to debate, and one central issue concerns the specific nature of the deficit. In particular, it is questioned whether the deficit is specific to speech and/or specific to temporal processing. To resolve this issue, a categorical perception identification task was administered in thirteen 11-year old dyslexic readers and 25 matched normal readers using 4 sound continua: (1) a speech contrast exploiting temporal cues (/bA/-/dA/), (2) a speech contrast defined by nontemporal spectral cues (/u/-/y/), (3) a nonspeech temporal contrast (spectrally rotated/bA/-/da/), and (4) a nonspeech nontemporal contrast (spectrally rotated/u/-/y/). Results indicate that children with dyslexia are less consistent in classifying speech and nonspeech sounds on the basis of rapidly changing (i.e., temporal) information whereas they are unimpaired in steady-state speech and nonspeech sounds. The deficit is thus restricted to categorizing sounds on the basis of temporal cues and is independent of the speech status of the stimuli. The finding of a temporal-specific but not speech-specific deficit in children with dyslexia is in line with findings obtained in adults using the same paradigm (Vandermosten et al., 2010, Proceedings of the National Academy of Sciences of the United States of America, 107: 10389-10394). Comparison of the child and adult data indicates that the consistency of categorization considerably improves between late childhood and adulthood, particularly for the continua with temporal cues. Dyslexic and normal readers show a similar developmental progress with the dyslexic readers lagging behind both in late childhood and in adulthood.

Modelling relations between sensory processing, speech perception, orthographic and phonological ability, and literacy achievement.

The general magnocellular theory postulates that dyslexia is the consequence of a multimodal deficit in the processing of transient and dynamic stimuli. In the auditory modality, this deficit has been hypothesized to interfere with accurate speech perception, and subsequently disrupt the development of phonological and later reading and spelling skills. In the visual modality, an analogous problem might interfere with literacy development by affecting orthographic skills. In this prospective longitudinal study, we tested dynamic auditory and visual processing, speech-in-noise perception, phonological ability and orthographic ability in 62 five-year-old preschool children. Predictive relations towards first grade reading and spelling measures were explored and the validity of the global magnocellular model was evaluated using causal path analysis. In particular, we demonstrated that dynamic auditory processing was related to speech perception, which itself was related to phonological awareness. Similarly, dynamic visual processing was related to orthographic ability. Subsequently, phonological awareness, orthographic ability and verbal short-term memory were unique predictors of reading and spelling development.

Auditory processing, speech perception and phonological ability in pre-school children at high-risk for dyslexia: a longitudinal study of the auditory temporal processing theory.

This study investigates whether the core bottleneck of literacy-impairment should be situated at the phonological level or at a more basic sensory level, as postulated by supporters of the auditory temporal processing theory. Phonological ability, speech perception and low-level auditory processing were assessed in a group of 5-year-old pre-school children at high-family risk for dyslexia, compared to a group of well-matched low-risk control children. Based on family risk status and first grade literacy achievement children were categorized in groups and pre-school data were retrospectively reanalyzed. On average, children showing both increased family risk and literacy-impairment at the end of first grade, presented significant pre-school deficits in phonological awareness, rapid automatized naming, speech-in-noise perception and frequency modulation detection. The concurrent presence of these deficits before receiving any formal reading instruction, might suggest a causal relation with problematic literacy development. However, a closer inspection of the individual data indicates that the core of the literacy problem is situated at the level of higher-order phonological processing. Although auditory and speech perception problems are relatively over-represented in literacy-impaired subjects and might possibly aggravate the phonological and literacy problem, it is unlikely that they would be at the basis of these problems. At a neurobiological level, results are interpreted as evidence for dysfunctional processing along the auditory-to-articulation stream that is implied in phonological processing, in combination with a relatively intact or inconsistently impaired functioning of the auditory-to-meaning stream that subserves auditory processing and speech perception.